After military service, Dover returned to Oxford and became Fellow and tutor at his old college in 1948. In 1955, Dover was appointed Professor of Greek at the University of St Andrews, and was twice Dean of the university's Faculty of Arts during his twenty-one years there.

He was elected to the Royal Society of Edinburgh in 1975. Dover received a knighthood two years later for services to Greek scholarship. In 1976, Dover became President of Corpus Christi College, Oxford, a post he held for ten years. During this tenure Dover was engaged in a protracted dispute with the college Librarian and a Fellow in History, Trevor Henry Aston (1925[1]–1985), who suffered from manic depression. Aston's erratic behaviour exasperated Dover and in Marginal Comment, his autobiography, he admitted: "it was clear to me by now that Trevor and the college must somehow be separated. My problem was one which I feel compelled to define with brutal candour: how to kill him without getting into trouble...I had no qualms about causing the death of a fellow from whose nonexistence the college would benefit, but I balked at the prospect of misleading a coroner's jury...consulting a lawyer to see if [I] would be legally at risk if [I] ignored a suicide call." Dover willingly put pressure on Aston and consorted with his doctor to ignore colleagues' expressions of concern. Aston was found dead in his rooms on 17 October 1985 after an overdose.[2]

Dover returned to St Andrews as the university's Chancellor in 1981. He was the first Chancellor in the University's history to be neither a peer nor an archbishop. Dover stepped down from the position after twenty-five years of service, effective 31 December 2005.

Dover's scholarly work focused especially on Thucydides, Aristophanes, and Plato, on the stylistics of Greek prose, and on Greek sexual morality. In addition to smaller editions of Thucydides books 6 and 7, he completed (with Anthony Andrewes) the fourth and fifth volumes of the Historical Commentary on Thucydides begun by A.W. Gomme and left unfinished at his death. (The complete work is often referred to as "Gomme-Andrewes-Dover.") His work on Aristophanes included two editions with commentary (on Clouds and Frogs) and a book on Aristophanic Comedy aimed at a more general readership.

His interest in stylistics stretches from his early study of Greek Word Order (1960) to his last major book, The Evolution of Greek Prose Style (1997). He had previously been responsible for supervising the second edition of J.D. Denniston's The Greek Particles (1950); though Dover is not named on the title page, his signed preface notes that he made various cuts, additions and changes. His series of Sather lectures on the corpus of speeches attributed to Lysias was important for its early application of stylometry to the study of Greek texts, as well as its agnostic conclusions. Since Athenian speechwriters adapted their style to the personality of their clients, Dover argued, it is difficult to make firm judgments about the authorship of speeches on the basis of style.

Dover's Greek Homosexuality (1978) marked a watershed in the study of classical Greek society, discussing topics such as pederasty and what he memorably called "intercrural copulation" in matter-of-fact terms. In particular, Dover made use of copious evidence from vase painting as a counterweight to the idealized picture of homoerotic relationships found in Plato.

Beyond his academic honours and pursuits, Dover was well known for his skill and devotion to bird watching and was considered one of Britain's finest birders.[4] As president of Corpus Christi College, Oxford in the 1970s and 80s he was impressive for being able to greet all Corpuscles by name. He achieved this by studying photographs and admitted to having occasional problems identifying new students when beards were in fashion.

Dover was the subject of an edition of the BBC Radio 4 programme "In the Psychiatrist's Chair", presented by Anthony Clare. He also featured in a BBC Television series "The Greeks", presented by Christopher Burstall.

In 1994 he published a controversial autobiography entitled "Marginal Comment". This prompted media attention[5] because of its frank description of his private life, and Dover's admission of wanting to murder one of the fellows of Corpus Christi College, the historian Trevor Aston.[6] Concerned about the effect that Aston's personal problems were having on the reputation of the college, Dover wrote that "It was clear to me that Trevor and the College must somehow be separated, and my problem was one which I feel compelled to define with brutal candour: how to kill him without getting into trouble." Aston later committed suicide.[7]

Dover resided in St Andrews, Fife, where he and his family have had a home since around 1960. He married Audrey Latimer in March 1947; Lady Dover died in December 2009 after 62 years of marriage. Dover died on 7 March 2010, survived by a son and daughter.[8][9]